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Marine Biology

, Volume 151, Issue 1, pp 293–299 | Cite as

Secondary metabolite and inorganic contents in Cystodytes sp. (Ascidiacea): temporal patterns and association with reproduction and growth

  • Susanna López-Legentil
  • Nataly Bontemps-Subielos
  • Xavier Turon
  • Bernard Banaigs
Research Article

Abstract

Temporal variation is one of the least known components of defence production in marine organisms. Here we examined whether there is a predictable temporal pattern in the production of chemical and structural defences by a marine invertebrate. To assess the seasonal variation in chemical defence, we measured ascididemin, the main pyridoacridine alkaloid in the blue Mediterranean morph of the ascidian Cystodytes sp. Structural defence variability was assessed on the basis of colony ash content, as it contains mainly spicules. Ascididemin concentration and the colony ash content displayed an annual cycle, reaching a minimum in spring and peaking in summer. Cross-correlation analyses with existing data on growth and reproduction suggested a significant trade-off between investment in reproduction and the other biological parameters considered (growth, inorganic content and ascididemin concentration). Our results suggest that optimization of resource allocation, probably influenced by biotic interactions and physical factors, shaped the temporal trends observed in secondary metabolite concentration and inorganic content.

Keywords

Biological Parameter Total Organic Matter Structural Defence Inorganic Content Larval Release 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Joseph R. Pawlik kindly made useful comments to improve this ms. Philippe Kerhervé (CEFREM) provided access to a 500°C oven. Diving assistance was provided by C. Menniti (University of Perpignan) and C. Palacin (University of Barcelona). F. Jamme helped with some laboratory work. This study was funded by the Interreg IIIA n. I3A-1-72-E program of the EU, by a Ministry of Education and Science/Fulbright grant to S.L-L., and the project CTM2004-05265 of the Spanish Government.

References

  1. Becerro MA, Paul VJ, Starmer J (1998) Intracolonial variation in chemical defences of the sponge Cacospongia sp. and its consequences on generalist fish predators and the specialist nudibranch predator Glossodoris pallida. Mar Ecol Prog Ser 168:187–196CrossRefGoogle Scholar
  2. Becerro MA, Turon X, Uriz MJ (1995) Natural variation of toxicity in encrusting sponge Crambe crambe (Schmidt) in relation to size and environment. J Chem Ecol 21:1931–1946CrossRefGoogle Scholar
  3. Boero F, Balduzzi A, Bavestrello G, Caffa B, Vietti RC (1986) Population dynamics of Eudendrium glomeratum (Cnidaria: Anthomedusae) on the Portofino Promontory (Ligurian Sea). Mar Biol 92:81–85CrossRefGoogle Scholar
  4. Bontemps N (1996) Noyau pyridoacridine, structure et synthèse d’alcaloïdes cytotoxiques isolés d’invértébres marins. PhD thesis, University of Perpignan, p 160Google Scholar
  5. Bracher F (1989) Total synthesis of the pentacyclic alkaloid ascididemin. Heterocycles 29:2093–2095CrossRefGoogle Scholar
  6. Burns E, Ilan M (2003) Comparison of anti-predatory defenses of Red Sea and Caribbean sponges. II. Physical defense. Mar Ecol Prog Ser 252:115–123CrossRefGoogle Scholar
  7. Coma R, Ribes M (2003) Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101:205–215CrossRefGoogle Scholar
  8. Coma R, Ribes M, Gili JM, Zabala M (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453CrossRefGoogle Scholar
  9. Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defence patterns in relation to defence theories. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, FL, pp 325–353CrossRefGoogle Scholar
  10. Dube D, Kim K, Aller AP, Harwell CD (2002) Size structure and geographic variation in chemical resistance of sea fan corals Gorgonia ventalina to a fungal pathogen. Mar Ecol Prog Ser 231:139–150CrossRefGoogle Scholar
  11. Fagerström T, Larsson S, Tenow O (1987) On optimal defence in plants. Funct Ecol 1:73–81CrossRefGoogle Scholar
  12. Harvell CD, Fenical W (1989) Chemical and structural defences of Caribbean gorgonians (Pseudopterogorgia spp.): intracolony localization of defence. Limnol Oceanogr 4:382–389CrossRefGoogle Scholar
  13. Harvell CD, Fenical W, Greene DH (1988) Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp.) I. Development of an in situ feeding assay. Mar Ecol Prog Ser 49:287–294CrossRefGoogle Scholar
  14. Harvell CD, Fenical W, Roussis V, Ruesink JL, Griggs CC, Greene CH (1993) Local and geographic variation in the defensive chemistry of a West Indian gorgonian coral (Briareum asbestinum). Mar Ecol Prog Ser 93:165–173CrossRefGoogle Scholar
  15. Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Berenbaum MR (ed) Marine and terrestrial chemical ecology, Academic Press Inc., New York, pp 371–413Google Scholar
  16. Karban R, Myers JH (1989) Induced plant responses to herbivory. Ann Rev Ecol Syst 20:331–348CrossRefGoogle Scholar
  17. Kobayashi J, Cheng J, Nakamura H, Ohizumi Y, Hirata Y, Sasaki T, Ohta T, Nozoe S (1988) Ascididemin, a novel pentacyclic aromatic alkaloid with potent antileukemic activity from the okinawan tunicate Didemnun sp. Tetrahedron Lett 29:1177–1180CrossRefGoogle Scholar
  18. Lambert G (1979) Early post-metamorphic growth, budding and spicule formation in the compound ascidian Cystodytes lobatus. Biol Bull 157:464–477CrossRefGoogle Scholar
  19. Lindquist N, Hay ME, Fenical W (1992) Defense of ascidians and their conspicuous larvae: adults vs larval chemical defenses. Ecol Monogr 62:547–568CrossRefGoogle Scholar
  20. López-Legentil S (2005) Multidisciplinary studies of the genus Cystodytes: from molecules to species. PhD Thesis, University of Barcelona, p 217Google Scholar
  21. López-Legentil S, Turon X (2005) How do morphotypes and chemotypes relate to genotypes? The colonial ascidian Cystodytes (Ascidiacea: Polycitoridae). Zool Scr 34:3–14CrossRefGoogle Scholar
  22. López-Legentil S, Turon X (2006) Population genetics, phylogeography and speciation of Cystodytes (Ascidiacea) in the western Mediterranean Sea. Biol J Linn Soc 88:203–214CrossRefGoogle Scholar
  23. López-Legentil S, Dieckmann R, Bontemps-Subielos N, Turon X, Banaigs B (2005a) Qualitative variation of alkaloids in colour morphs of Cystodytes (Ascidiacea). Biochem Syst Ecol 33(11):1107–1119CrossRefGoogle Scholar
  24. López-Legentil S, Ruchy M, Domenech A, Turon X (2005b) Life cycles and growth rates of two morphotypes of Cystodytes (Ascidiacea) in the western Mediterranean. Mar Ecol Prog Ser 296:219–228CrossRefGoogle Scholar
  25. López-Legentil S, Bontemps-Subielos N, Turon X, Banaigs B (2006a) Temporal variation in the production of four secondary metabolites in a colonial ascidian. J Chem Ecol 32:2079–2084CrossRefGoogle Scholar
  26. López-Legentil S, Turon X, Schupp P (2006b) Chemical and physical defences against predators in Cystodytes (Ascidiacea). J Exp Mar Biol Ecol 332(1):27–36CrossRefGoogle Scholar
  27. Maida M, Carroll AR, Coll JC (1993) Variability of terpene contents in the soft coral (Coelenterata: Octocorallia), and its ecological implications. J Chem Ecol 19:2285–2298CrossRefGoogle Scholar
  28. McClintock JB, Amsler MO, Amsler CD, Southworth KJ, Petrie C, Baker BJ (2004) Biochemical composition, energy content and chemical antifeedant and antifoulant defenses of the colonial Antarctic ascidian Distaplia cylindrical. Mar Biol 145:885–894CrossRefGoogle Scholar
  29. McClintock JB, Baker BJ (2001) Marine chemical ecology. CRC Press, Boca Raton, FLCrossRefGoogle Scholar
  30. McClintock JB, Heine J, Slattery M, Weston J (1991) Biochemical and energetic composition, population biology, and chemical defense of the antarctic ascidian Cnemidocarpa verrucosa lesson. J Exp Mar Bio Ecol 147:163–175CrossRefGoogle Scholar
  31. O’Neal W, Pawlik JR (2002) A reappraisal of the chemical and physical defenses of Caribbean gorgonian corals against predatory fishes. Mar Ecol Prog Ser 240:117–126CrossRefGoogle Scholar
  32. Page M, West L, Northcote P, Battershill C, Kelly M (2005) Spatial and temporal variability of cytotoxic metabolites in populations of the New Zealand sponge Mycale hentscheli. J Chem Ecol 31(5):1161–1174CrossRefGoogle Scholar
  33. Paul VJ, Puglisi MP, Ritson-Williams R (2006) Marine chemical ecology. Nat Prod Rep 23:153–180CrossRefGoogle Scholar
  34. Paul VP, Van Alstyne KL (1988) Chemical defence and chemical variation in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta). Coral Reefs 6:263–269CrossRefGoogle Scholar
  35. Pavia H, Toth G, Åberg P (1999) Trade-offs between phlorotannin production and annual growth in natural populations of the brown seaweed Ascophyllum nodosum. J Ecol 87(5):761–771CrossRefGoogle Scholar
  36. Puglisi MP, Paul VJ, Biggs J, Slattery M (2002) Co-occurrence of chemical and structural defenses in gorgonian corals from Guam. Mar Ecol Prog Ser 239:105–114CrossRefGoogle Scholar
  37. Rhoades DF (1979) Evolution of plant chemical defence against herbivores. In: Rosenthal GA (ed) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 3–54Google Scholar
  38. Ribes M, Coma R, Gili JM (1998) Seasonal variation of in situ feeding rates by the temperate ascidian Halocynthia papillosa. Mar Ecol Prog Ser 175:201–213CrossRefGoogle Scholar
  39. Schmitz FJ, DeGuzman FS, Hossain MB, van der Helm D (1991) Cytotoxic aromatic alkaloids from the ascidian Amphicarpa meridiana and Leptoclinides sp.: meridine and 11-Hydroxyascididemin. J Org Chem 56:804–808CrossRefGoogle Scholar
  40. Schupp P, Eder C, Paul VJ, Proksch P (1999) Distribution of secondary metabolites in the sponge Oceanapia sp. and its ecological implications. Mar Biol 135:573–580CrossRefGoogle Scholar
  41. Sebens KP (1986) Spatial relationships among encrusting marine organisms in the New England subtidal zone. Ecol Monogr 56:73–96CrossRefGoogle Scholar
  42. Seiderer LJ, Newell RC (1988) Exploitation of phytoplankton as a food resource by the kelp bed ascidian Pyura stolonifera. Mar Ecol Prog Ser 50:107–115CrossRefGoogle Scholar
  43. Skogsmyr I, Fagerström T (1992) The cost of anti-herbivory defence: an evaluation of some ecological and physiological factors. Oikos 64:451–457CrossRefGoogle Scholar
  44. Steinberg PD (1995) Seasonal variation in the relationship between growth rate and phlorotannin production in the kelp Ecklonia radiata. Oecologia 102(2):169–173CrossRefGoogle Scholar
  45. Steinberg PD, van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222CrossRefGoogle Scholar
  46. Svane I, Young CM (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol Ann Rev 27:45–90Google Scholar
  47. Tarjuelo I, López-Legentil S, Codina M, Turon X (2002) Defence mechanisms of adults and larvae of marine invertebrates: patterns of toxicity and palatability in colonial ascidians. Mar Ecol Prog Ser 235:103–115CrossRefGoogle Scholar
  48. Tarjuelo I, Turon X (2004) Resource allocation in ascidians: reproductive investment vs. other life-history traits. Inv Biol 123:168–180Google Scholar
  49. Turon X, Becerro MA (1992) Growth and survival of several ascidian species from the northwestern Mediterranean. Mar Ecol Prog Ser 82:235–247CrossRefGoogle Scholar
  50. Turon X, Becerro MA, Uriz MJ (1996) Seasonal patterns of toxicity in benthic invertebrates: the encrusting sponge Crambe crambe (Poecilosclerida). Oikos 75:33–40CrossRefGoogle Scholar
  51. Underwood AJ, Chapman MG, Connell SD (2000) Observations in ecology: you can’t make progress on processes without understanding the patterns. J Exp Mar Biol Ecol 250:97–115CrossRefGoogle Scholar
  52. Uriz MJ, Turon X, Becerro MA, Galera J (1996) Feeding deterrence in sponges. The role of toxicity, physical defenses, energetic contents, and life-history stage. J Exp Mar Biol Ecol 205:187–204CrossRefGoogle Scholar
  53. Valls R, Banaigs B, Piovetti L, Zerzouf A (1993) Variations géographiques de la composition en diterpènes de Bifurcaria bifurcata des côtes atlantiques marocaines. Ann Inst Océanogr 69:215–223Google Scholar
  54. Van Alstyne KL, Wylie CR, Paul VJ (1994) Antipredator defences in tropical Pacific soft corals (Coelenterata: Alcyonacea). II. The relative importance of chemical and structural defences in three species of Sinularia. J Exp Mar Biol Ecol 178:17–34CrossRefGoogle Scholar
  55. Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766CrossRefGoogle Scholar
  56. Young CM, Bingham BL (1987) Chemical defense and aposematic coloration in larvae of the ascidian Ecteinascidia turbinata. Mar Biol 96:539–544CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Susanna López-Legentil
    • 1
    • 2
    • 3
  • Nataly Bontemps-Subielos
    • 2
  • Xavier Turon
    • 1
  • Bernard Banaigs
    • 2
  1. 1.Department of Animal Biology (Invertebrates), Faculty of BiologyUniversity of BarcelonaBarcelonaSpain
  2. 2.Laboratoire de Chimie des Biomolécules et de l’EnvironnementUniversity of PerpignanPerpignanFrance
  3. 3.Centre for Marine ScienceUniversity of North Carolina at WilmingtonWilmingtonUSA

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